Phosphorylation regulates the subcellular location and activity of the snail transcriptional repressor

Molecular and Cellular Biology

Volumn 23, Issue 14, 2003, Pages 5078-5089

  Domínguez, David ^a   Montserrat Sentís, Bàrbara ^a   Virgós Soler, Ariadna ^a   Guaita, Sandra ^a   Grueso, Judit ^a   Porta, Montserrat ^a   Puig, Isabel ^a   Baulida, Josep ^a   Francí, Clara ^a   García de Herreros, Antonio ^a,b  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b INST MUNIC D INVESTIGACIO MEDICA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; UVOMORULIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL MIGRATION; CELL SUSPENSION; CELLULAR DISTRIBUTION; EPITHELIUM CELL; EPITHELIUM TUMOR; EXTRACELLULAR MATRIX; NONHUMAN; PHASE TRANSITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; SNAIL; TRANSCRIPTION REGULATION; ZINC FINGER MOTIF;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; BASE SEQUENCE; CELL NUCLEUS; CYTOSOL; DNA-BINDING PROTEINS; EXTRACELLULAR MATRIX; HUMANS; KARYOPHERINS; LEUCINE; MICE; MOLECULAR SEQUENCE DATA; NUCLEAR LOCALIZATION SIGNALS; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECEPTORS, CYTOPLASMIC AND NUCLEAR; REPRESSOR PROTEINS; SERINE; SUBCELLULAR FRACTIONS; TRANSCRIPTION FACTORS; TUMOR CELLS, CULTURED;

ANIMALIA; GASTROPODA; NES;

EID: 0038450250     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.14.5078-5089.2003     Document Type: Article

References (47)

1. Barker, N., and H. Clevers. 2001. Tumor environment: a potent driving force in colorectal cancer? Trends Mol. Med. 7:535-537.
2. Batlle, E., E. Sancho, C. Francí, D. Domínguez, M. Monfar, J. Baulida, and A. García de Herreros. 2000. The transcription factor Snail is a repressor of E-cadherin gene expression in epithelial tumor cells. Nat. Cell Biol. 2:84-89.
3. Beals, C. R., N. A. Clipstone, S. N. Ho, and G. R. Crabtree. 1997. Nuclear localization of NFA-Tc by a calcineurin-dependent, cyclosporin-sensitive intramolecular interaction. Genes Dev. 11:824-834.
4. Blanco, M. J., G. Moreno-Bueno, D. Sarrio, A. Locascio, A. Cano, J. Palacios, and M. A. Nieto. 2002. Correlation of Snail expression with histological grade and lymph node status in breast carcinomas. Oncogene 21:3241-3246.
5. Brabletz, T., A. Jung, S. Reu, M. Pozner, F. Hulbek, L. A. Kunz-Schugart, R. Knuechtel, and T. Kirchner. 2001. Variable β-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment. Proc. Natl. Acad. Sci. USA 98:10356-10361.
6. Cano, A., M. A. Pérez-Moreno, I. Rodrigo, A. Locascio, M. J. Blanco, M. G. del Barrio, F. Portillo, and M. A. Nieto. 2000. The transcription factor Snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2:78-83.
7. Carver, E. A., J. Rulang, Y. Lan, K. F. Oram, and T. Gridley. 2001. The mouse Snail gene encodes a key regulator of the epithelial-mesenchymal transition. Mol. Cell. Biol. 21:8184-8188.
8. Cheng, C. W., P. E. Wu, J. C. Yu, C. S. Huang, C. T. Yue, C. W. Wu, and C. Y. Shen. 2001. Mechanisms of inactivation of E-cadherin in breast carcinoma: modification of the two-hit hypothesis of tumor suppressor gene. Oncogene 20:3814-3823.
9. Comijn, J., G. Berx, P. Vermassen, K. Verschuren, L. van Grunsven, E. Bruyneel, M. Mareel, D. Huylebroek, and F. van Roy. 2001. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol. Cell 7:1267-1278.
10. Engel, K., A. Kotlyarov, and M. Gaestel. 1998. Leptomycin B-sensitive nuclear export of MAPKAP kinase 2 is regulated by phosphorylation. EMBO J. 17:3363-3371.
11. Fornerod, M., M. Ohno, M. Yoshida, and I. W. Mattaj. 1997. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90:1051-1060.
12. Fukuda, M., S. Asano, T. Nakamura, M. Adachi, M. Yoshida, M. Yanagida, and E. Nishida. 1997. CRM1 is responsible for intracellular transport mediated by the nuclear export signal. Nature 390:308-310.
13. Gama-Carvalho, M., R. D. Krauss, L. Chiang, J. Valcárcel, M. R. Green, and M. Carmo-Fonseca. 1997. Targeting U2AF65 to sites of active splicing in the nucleus. J. Cell Biol. 197:975-987.
14. Guaita, S., I. Puig, C. Franci, M. Garrido, D. Dominguez, E. Batlle, E. Sancho, S. Dedhar, A. Garcia de Herreros, and J. Baulida. 2002. Snail induction of epithelial-to-mesenchymal transition in tumor cells is accompanied by MUC-1 repression and ZEB1 expression. J. Biol. Chem. 277:30209-39216.
15. Hajra, K. M., D. Y. Chen, and E. R. Fearon. 2002. The SLUG zinc finger protein represses E-cadherin in breast. Cancer Res. 62:1613-1618.
16. Hemavathy, K., S. I. Ashraf, and Y. T. Ip. 2000. Snail/Slug family of repressors: slowly going into the fast lane of development and cancer. Gene 257: 1-12.
17. Hemavathy, K., S. C. Guru, J. Harris, J. D. Chen, and Y. T. Ip. 2000. Human Slug is a repressor that localizes to sites of active transcription. Mol. Cell. Biol. 26:5087-5095.
18. kip1 on serine 10 is required for its binding to CRM1 and nuclear export. J. Biol. Chem. 277:14355-14358.
19. Jiao, W., K. Miyazaki, and Y. Kitajima. 2002. Inverse correlation between E-cadherin and Snail expression in hepatocellular carcinoma cell lines in vitro and in vivo. Br. J. Cancer 86:98-101.
20. Kudo, N., B. Wolff, T. Sekimoto, E. P. Schreiner, Y. Yoneda, M. Yanagida, S. Horinouchi, and M. Yoshida. 1998. Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1. Exp. Cell Res. 242:540-547.
21. Lischka, P., O. Rosorius, E. Trommer, and T. Stamminger. 2001. A novel transferable nuclear export signal mediates CRM1-independent nucleocytoplasmic shuttling of the human cytomegalovirus transactivator protein pUL69. EMBO J. 20:7271-7283.
22. Lochter, A., and M. J. Bissell. 1995. Involvement of extracellular matrix in breast cancer. Semin. Cancer Biol. 6:165-173.
23. Lochter, A., S. Galosy, J. Muschler, N. Freedman, Z. Werb, and M. J. Bissell. 1997. Matrix metalloproteinase stromelysin-1 triggers a cascade of molecular alterations that leads to stable epithelial-to-mesenchymal conversion and a premalignant phenotype in mammary epithelial cells. J. Cell Biol. 139:1861-1872.
24. Manzanares, M., A. Locascio, and M. A. Nieto. 2001. The increasing complexity of the Snail gene superfamily in metazoan evolution. Trends Gen. 17:178-181.
25. Mauhin, V., Y. Lutz, C. Dennefeld, and A. Auberga. 1993. Definition of the DNA-binding site repertoire for the Drosophila transcription factor SNAIL. Nucleic Acids Res. 21:3951-3957.
26. Menke, A., C. Philippi, R. Vogelmann, B. Seidel, M. P. Lutz, G. Adler, and D. Wedlich. 2001. Down-regulation of E-cadherin gene expression by collagen type I and type III in pancreatic cancer cell lines. Cancer Res. 61:3508-3517.
27. Middeler, G., K. Zerf, S. Jenovai, A. Thulig, M. Tschodrich-Rotter, U. Kubitscheck, and R. Peters. 1997. The tumor suppressor p53 is subject to both nuclear import and export, and both are fast, energy-dependent and lectin-inhibited. Oncogene 14:1407-1417.
28. Miravet, S., J. Piedra, F. Miró, E. Itarte, A. García de Herreros, and M. Duñach. 2002. The transcriptional factor Tcf-4 contains different binding sites for β-catenin and plakoglobin. J. Biol. Chem. 277:1884-1891.
29. Nieto, M. A. 2002. The Snail superfamily of Zinc finger transcription factors. Nat. Rev. Mol. Cell. Biol. 3:155-166.
30. Nishi, K., M. Yoshida, D. Fujiwara, M. Nishikawa, S. Horinouchi, and T. Beppu. 1994. Leptomycin B targets a regulatory cascade of CRM1, a fission yeast nuclear protein, involved in control of higher order chromosome structure and gene expression. J. Biol. Chem. 269:6320-6324.
31. Okamura, H., J. Aramburu, C. García-Rodríguez, J. P. B. Viola, A. Raghavan, M. Tahiliani, X. Zhang, J. Qin, P. G. Hogan, and A. Rao. 2000. Concerted dephosphorylation of the transcription factor NFAT1 induces a conformational switch that regulates transcriptional activity. Mol. Cell 6:539-550.
32. Perl, A. K., P. Wilgenbus, U. Dahl, H. Semb, and G. Christofori. 1998. A causal role for E-cadherin in the translation from adenoma to carcinoma. Nature 392:190-193.
33. Poser, I., D. Dominguez, A. García de Herreros, A. Varnai, R. Buettner, and A. K. Bosserhoff. 2001. Loss of E-cadherin expression in melanoma cells involves upregulation of the transcriptional factor Snail. J. Biol. Chem. 276:24661-24666.
34. Rosivatz, E., I. Becker, K. Specht, E. Fricke, B. Luber, R. Busche, H. Hofler, and K. F. Becker. 2002. Different expression of the epithelial-mesenchymal transition regulators Snail, SIP1, and Twist in gastric cancer. Am. J. Pathol. 161:1881-1891.
35. Sefton, B. M. 1995. Phosphoamino acid analysis, p. 13.3.1-13.3.8. In J. E. Coligan, B. M. Dunn, H. L. Ploegh, D. W. Speicher, and P. T. Wingfield (ed.), Current protocols in protein science. John Wiley & Sons, Inc., New York, N.Y.
36. Spector, D. L. 2001. Nuclear domains. J. Cell Sci. 114:2891-2893.
37. Spector, D. L., X. D. Fu, and T. Maniatis. 1991. Association between distinct pre-mRNA splicing components and the cell nucleus. EMBO J. 10:3467-3481.
38. Stommel, J. M., N. D. Marchenko, G. S. Jimenez, U. M. Moll, T. J. Hope, and G. M. Wahl. 1999. A leucine-rich nuclear export signal in the p53 tetramerization domain: regulation of subcellular localization and p53 activity by NES masking. EMBO J. 18:1660-1672.
39. Sussman, J., D. Stokoe, N. Ossina, and E. Shtivelman. 2001. Protein kinase B phosphorylates AHNAK and regulates its subcellular location. J. Cell Biol. 154:1019-1030.
40. Tan, C., P. Costello, J. Sanghera, D. Domínguez, J. Baulida, A. García de Herreros, and S. Dedhar. 2001. Inhibition of integrin linked kinase (ILK) suppresses β-catenin-Lef-1/TFcf-dependent transcription and expression of the E-cadherin repressor, snail, in APC -/- human colon carcinoma cells. Oncogene 20:133-140.
41. Ullman, K. S., M. A. Powers, and D. J. Forbes. 1997. Nuclear export receptors: from importin to exportin. Cell 90:967-970.
42. Vleminckx, K., L. Vakaet, M. Mareel, W. Fiers, and F. Van Roy. 1991. Genetic manipulation of E-cadherin expression by epithelial tumor cells reveals an invasion suppressor role. Cell 77:1605-1613.
43. Wu, C., S. Y. Keightley, C. Leung-Hagesteijn, G. Radeva, M. Coppolino, S. Goicoechea, J. A. McDonald, and S. Dedhar. 1998. Integrin-linked kinase regulates fibronectin matrix assembly, E-cadherin expression, and tumorigenicity. J. Biol. Chem. 273:528-536.
44. Yokoyama, K., N. Kamata, E. Hayashi, T. Hoteiya, N. Ueda, R. Fujimoto, and M. Nagayama. 2001. Reverse correlation of E-cadherin and Snail expression in oral squamous cell carcinoma cells in vitro. Oral Oncol. 37:65-71.
45. Yokoyama, K., N. Kamata, R. Fujimoto, S. Tsutsumi, M. Tomomari, M. Takai, H. Hoshokawa, and M. Nagayama. 2003. Increased invasion and matrix metalloproteinase-2 expression by Snail-induced mesenchymal transition in squamous cell carcinomas. Int. J. Oncol. 22:891-898.
46. Zhang, Y., and Y. Xiong. 2001. A p53 amino-terminal nuclear export signal inhibited by DNA damage-induced phosphorylation. Science 292:1910-1915.
47. Zhu, J., and F. McKeon. 1999. NF-AT activation requires suppression of CRM1-dependent export by calcineurin. Nature 398:256-260.